Hostname: page-component-848d4c4894-8bljj Total loading time: 0 Render date: 2024-07-05T08:47:47.226Z Has data issue: false hasContentIssue false
  • English
  • Français

Beyond a gut feeling: How the immune system impacts the effect of gut microbiota in neurodevelopment

Published online by Cambridge University Press:  15 July 2019

Atiqah Azhari Open the ORCID record for Atiqah Azhari [Opens in a new window] ,
Farouq Azizan  and
Gianluca Esposito
Atiqah Azhari
Affiliation:
Social and Affiliative Neuroscience Lab, Psychology Program, Nanyang Technological University, S-639798Singapore. atiqah.azhari.09@gmail.comfarouqazizan@gmail.comhttps://www.linkedin.com/in/atiqah-azhari/https://www.linkedin.com/in/muhammadfarouqbinazizan/https://blogs.ntu.edu.sg/sanlab/
Farouq Azizan
Affiliation:
Social and Affiliative Neuroscience Lab, Psychology Program, Nanyang Technological University, S-639798Singapore. atiqah.azhari.09@gmail.comfarouqazizan@gmail.comhttps://www.linkedin.com/in/atiqah-azhari/https://www.linkedin.com/in/muhammadfarouqbinazizan/https://blogs.ntu.edu.sg/sanlab/
Gianluca Esposito
Affiliation:
Social and Affiliative Neuroscience Lab, Psychology Program, Nanyang Technological University, S-639798Singapore. atiqah.azhari.09@gmail.comfarouqazizan@gmail.comhttps://www.linkedin.com/in/atiqah-azhari/https://www.linkedin.com/in/muhammadfarouqbinazizan/https://blogs.ntu.edu.sg/sanlab/ Affiliative Behaviour and Physiology Lab, Department of Psychology and Cognitive Sciences, University of Trento, Trento I-38068, Italy. gesposito79@gmail.comhttp://abp.dipsco.unitn.it/
Get access Rights & Permissions [Opens in a new window]

Abstract

Hooks et al. posit that gastrointestinal microbes alter the end state of development indirectly. Here, we present the immune system as the link that facilitates communication between the gut and the brain. Illustrating the case of autism spectrum disorder, we explicate the role of the immune system in responding to microbial dysbiosis by inducing an inflammatory state that affects neurodevelopment. We propose two models: directly, within the infant, and indirectly, via maternal and infant systems.

Type
Open Peer Commentary
Information
Behavioral and Brain Sciences , Volume 42 , 2019 , e64
Check for updates
Copyright
Copyright © Cambridge University Press 2019 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

American Psychiatric Association (2013) Diagnostic and statistical manual of mental disorders (DSM-5). American Psychiatric Association.Google Scholar
Ashwood, P. & Wakefield, A. J. (2006) Immune activation of peripheral blood and mucosal CD3+ lymphocyte cytokine profiles in children with autism and gastrointestinal symptoms. Journal of Neuroimmunology 173(1–2):126–34.Google Scholar
Azhari, A., Farouq, M. & Esposito, G. (2018) A systematic review of gut-immune-brain mechanisms in autism spectrum disorder. Developmental Psychobiology. Available at: https://doi.org/10.1002/dev.21803.Google Scholar
Breese, E. J., Michie, C. A., Nicholls, S. W., Murch, S. H., Williams, C. B., Domizio, P., Walker-Smith, J. A. & Macdonald, T. T. (1994) Tumor necrosis factor α-producing cells in the intestinal mucosa of children with inflammatory bowel disease. Gastroenterology 106(6):1455–66.Google Scholar
Carabotti, M., Scirocco, A., Maselli, M. A. & Severi, C. (2015) The gut-brain axis: Interactions between enteric microbiota, central and enteric nervous systems. Annales de Gastroenterologie et D'hepatologie 28(2):203–209.Google Scholar
El-Ansary, A. & Al-Ayadhi, L. (2014) GABAergic/glutamatergic imbalance relative to excessive neuroinflammation in autism spectrum disorders. Journal of Neuroinflammation 11:189.Google Scholar
Erny, D., Hrabě de Angelis, A. L., Jaitin, D., Wieghofer, P., Staszewski, O., David, E., Keren-Shaul, H., Mahlakoiv, T., Jakobshagen, K., Buch, T., Schwierzeck, V., Utermöhlen, O., Chun, E., Garrett, W. S., McCoy, K. D., Diefenbach, A., Staeheli, P., Stecher, B., Amit, I. & Prinz, M. (2015) Host microbiota constantly control maturation and function of microglia in the CNS. Nature Neuroscience 18(7):965–77.Google Scholar
Fernández de Cossío, L., Guzmán, A., van der Veldt, S. & Luheshi, G.N. (2017) Prenatal infection leads to ASD-like behavior and altered synaptic pruning in the mouse offspring. Brain, Behavior, and Immunity 63:88–98.Google Scholar
Finegold, S. M., Molitoris, D., Song, Y., Liu, C., Vaisanen, M.-L., Bolte, E., McTeague, M., Sandler, R., Wexler, H., Marlowe, E. M., Collins, M. D., Lawson, P. A., Summanen, P., Baysallar, M., Tomzynski, T. J., Read, E., Johnson, E., Rolfe, R., Nasir, P., Shah, H., Haake, D. A., Manning, P. & Kaul, A. (2002) Gastrointestinal microflora studies in late-onset autism. Clinical Infectious Diseases 35(S1):S6–16.Google Scholar
Gilmore, J. H., Jarskog, L. F. & Vadlamudi, S. (2005) Maternal poly I:C exposure during pregnancy regulates TNF alpha, BDNF, and NGF expression in neonatal brain and the maternal-fetal unit of the rat. Journal of Neuroimmunology 159(1–2):106–12.Google Scholar
Kang, D.-W., Park, J. G., Ilhan, Z. E., Wallstrom, G., Labaer, J., Adams, J. B. & Krajmalnik-Brown, R. (2013) Reduced incidence of Prevotella and other fermenters in intestinal microflora of autistic children. PLoS ONE 8(7):e68322.Google Scholar
Khakzad, M. R., Javanbakht, M., Shayegan, M. R., Kianoush, S., Omid, F., Hojati, M. & Meshkat, M. (2012) The complementary role of high sensitivity C-reactive protein in the diagnosis and severity assessment of autism. Research in Autism Spectrum Disorders 6(3):1032–37.Google Scholar
Kim, S., Kim, H., Yim, Y. S., Ha, S., Atarashi, K., Tan, T. G., Longman, R. S., Honda, K., Littman, D. R., Choi, G. B. & Huh, J. R. (2017b) Maternal gut bacteria promote neurodevelopmental abnormalities in mouse offspring. Nature 549(7673):528–32.Google Scholar
Li, X., Chauhan, A., Sheikh, A. M., Patil, S., Chauhan, V., Li, X.-M., Ji, L., Brown, T. & Malik, M. (2009) Elevated immune response in the brain of autistic patients. Journal of Neuroimmunology 207(1–2):111–16.Google Scholar
Qin, L., Wu, X., Block, M. L., Liu, Y., Breese, G. R., Hong, J.-S., Knapp, D. J. & Crews, F. T. (2007) Systemic LPS causes chronic neuroinflammation and progressive neurodegeneration. GLIA 55(5):453–62.Google Scholar
Rodriguez, J. I. & Kern, J. K. (2011) Evidence of microglial activation in autism and its possible role in brain underconnectivity. Neuron Glia Biology 7(2–4):205–13.Google Scholar
Takano, T. (2015) Role of microglia in autism: Recent advances. Developmental Neuroscience 37(3):195–202.Google Scholar
Tetreault, N. A., Hakeem, A. Y., Jiang, S., Williams, B. A., Allman, E., Wold, B. J. & Allman, J. M. (2012) Microglia in the cerebral cortex in autism. Journal of Autism and Developmental Disorders 42(12):2569–84.Google Scholar
Torrente, F., Ashwood, P., Day, R., Machado, N., Furlano, R. I., Anthony, A., Davies, S. E., Wakefield, A. J., Thomson, M. A., Walker-Smith, J. A. & Murch, S. H. (2002) Small intestinal enteropathy with epithelial IgG and complement deposition in children with regressive autism. Molecular Psychiatry 7:375–82.Google Scholar
Vargas, D. L., Nascimbene, C., Krishnan, C., Zimmerman, A. W. & Pardo, C. A. (2004) Neuroglial activation and neuroinflammation in the brain of patients with autism. Annals of Neurology 57(1):67–81.Google Scholar